diagnostic evaluation and short term outcome as indicators of long term prognosis in horses with findings suggestive of inflammatory bowel disease treated with corticosteroids and anthelmintics

R E S E A R C H Open AccessDiagnostic evaluation and short-term outcome as indicators of long-term prognosis in horses with findings suggestive of inflammatory bowel disease treated with

R E S E A R C H Open Access

Diagnostic evaluation and short-term outcome as indicators of long-term prognosis in horses with findings suggestive of inflammatory bowel disease treated with corticosteroids and anthelmintics

Ritva Kaikkonen1,4, Kati Niinistö1*, Benjamin Sykes2, Marjukka Anttila3, Satu Sankari1and Marja Raekallio1

Abstract

Background: Recurrent colic and unexplained weight loss despite good appetite and adequate feeding and management practices are common conditions in the horse However, little information has been published

on the systematic diagnostic evaluation, response to treatment, prognostic factors or outcome of either presentation The aims of this study were to 1) identify possible prognostic indicators and 2) report the short- and long-term response

to treatment with corticosteroid therapy of a variety of horses with a presumptive diagnosis of inflammatory bowel disease (IBD)

Thirty-six horses with a history of recurrent colic and/or unexplained weight loss were screened with a detailed clinical, clinicopathological and diagnostic imaging examination Twenty horses were subsequently selected that had findings consistent with inflammatory bowel disease based on the fulfilment of one or more of the following additional inclusion criteria: hypoproteinaemia, hypoalbuminaemia, malabsorption, an increased intestinal wall thickness on ultrasonographic examination or histopathological changes in rectal biopsy These 20 horses were treated with a standardized larvicidal anthelmintic regime and a minimum of three weeks of corticosteroid therapy

Results: The initial response to treatment was good in 75% (15/20) of horses, with a 3-year survival rate of 65% (13/20) The overall 3-year survival in horses that responded to initial treatment (12/15) was significantly higher (P = 0.031) than in those that did not respond to initial treatment (1/5) The peak xylose concentration was significantly (P = 0.048) higher in survivors (1.36 ± 0.44 mmol/L) than non-survivors (0.94 ± 0.36 mmol/L)

Conclusions: The overall prognosis for long-term survival in horses with a presumptive diagnosis of IBD appears

to be fair to moderate, and the initial response to anthelmintic and corticosteroid therapy could be a useful prognostic indicator The findings of the present study suggest that a low peak xylose concentration in absorption testing is associated with a less favourable prognosis, supporting the use of this test

Keywords: Horse, Weight loss, Colic, IBD, Total protein, Albumin, D-xylose

Background

Recurrent colic and weight loss are conditions in the horse

that can present either in combination or as separate

problems Numerous reasons exist for both presentations,

including management and feeding practices, intestinal

diseases such as parasitism and neoplasias [1,2] and

various non-intestinal diseases [1] Inflammatory bowel

disease (IBD) is another potential cause of both recurrent colic and weight loss that has been histologically classified into the different subtypes of lymphocytic-plasmacytic enterocolitis (LPE), granulomatous enteritis (GE), mul-tisystemic eosinophilic epitheliotropic disease (MEED), diffuse eosinophilic enteritis (DEE) and idiopathic focal eosinophilic enteritis (IFEE) [3-6] IBD has previously been reported to cause a variety of clinical presentations, from malabsorption and weight loss to diarrhoea and colic In particular, eosinophilic enteritis has been reported

* Correspondence: kati.niinisto@helsinki.fi

1

Department of Equine and Small Animal Medicine, Faculty of Veterinary

Medicine, University of Helsinki, P.O Box 57, FI-00014 Helsinki, Finland

Full list of author information is available at the end of the article

© 2014 Kaikkonen et al.; licensee BioMed Central Ltd This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this

to cause colic, while weight loss, hypoproteinaemia,

hypo-albuminaemia and carbohydrate malabsorption have all

been associated with LPE, MEED and GE [4,5]

Currently, diagnostic evaluation of equine gastrointestinal

disease includes clinical and dental examination, routine

haematology and biochemistry Where these fail to identify

the pathology, abdominal ultrasonography, carbohydrate

absorption tests and histopathology of rectal mucosal

biopsies may be useful [1] The use of rectal mucosal

biopsies is appealing, as they are minimally invasive

and easy to obtain with no specialized equipment, and

histopathology has been demonstrated to be potentially

useful in determining the underlying disease process

[7,8] Alternatively, gastric and duodenal mucosal biopsies

can be taken via endoscopy, or full thickness intestinal

biopsies can be taken via exploratory celiotomy However,

these require specialized equipment that is not always

available or affordable, which limits their usefulness

Indirect tests of intestinal function, such as D-xylose

and glucose absorption, have been described in the horse

These tests can provide useful information, particularly on

small intestinal function The D-xylose absorption test is

considered more accurate than the glucose absorption

test, because D-xylose is not normally present in the horse

and the serum concentration of D-xylose is not affected

by factors such as metabolic status, stress or excitement,

in contrast to glucose [1,9-13]

The retrospective evaluation of horses with weight loss

has recently been reported by Metcalfe et al [14], but

at present there is a paucity of systematic prospective

studies evaluating the results, and identification of risk

factors, from routine examination (history and clinical

evaluation), measurement of carbohydrate absorption,

abdominal ultrasonography and histopathological

find-ings from rectal biopsy in horses with recurrent colic

or weight loss Furthermore, limited information exists

regarding the treatment response of various enteropathies

to corticosteroid therapy, although the prognosis of IBD is

generally regarded as guarded to poor [4,8,15-17] Finally,

the long-term prognosis for horses with a presumptive

diagnosis of IBD that respond to initial treatment with

corticosteroid therapy has not yet been reported

The aims of the study were to 1) identify prognostic

in-dicators and 2) report the short- and long-term response

of a variety of horses with signs suggestive of IBD to

treat-ment with corticosteroid and anthelmintic therapy

Methods

Horses

The prospective cohort clinical study was performed

between 1 May 2004 and 31 December 2005 at the

Equine Hospital of the Faculty of Veterinary Medicine,

University of Helsinki, and Hyvinkää Equine Hospital,

Finland Long-term survival was reported for a 3-year

period following the discontinuation of treatment Horses with a history of recurrent colic, as defined by at least two episodes of colic requiring veterinary attention during the preceding 12 months [18], or anamnestic information regarding unexplained weight loss or an inability to gain weight despite adequate feeding and management practices, were considered eligible for initial screening for inclusion

in the study Furthermore, to be eligible for screening, horses were required to be ≥2 years of age and have received adequate feeding, deworming and dental care

as determined by the examining veterinarian Horses that presented with acute colic or that had previously undergone colic surgery were excluded, as were horses receiving corticosteroid therapy at the time of assessment

or in the six months preceding assessment The study was approved by the Ethical Committee of the University of Helsinki (UH number 89–04) Informed consent from the owner, or the trainer acting as an agent for the owner, was obtained at the time of enrolment in the study

Diagnostic evaluation

A thorough history was obtained, including signalment and management The initial examination included a basic clin-ical examination, determination of body weight with scales, lameness examination, oral examination, palpation per rectum, a complete blood count, fibrinogen measurement, serum biochemistry (globulins were counted by subtracting serum albumin from total protein), thoracic and abdominal radiography, transabdominal ultrasonography, peritoneal fluid analysis, urinalysis, a faecal flotation test for parasites,

a D-xylose absorption test [19], gastroscopy and duode-noscopy [20], as well as a rectal mucosal biopsy and histopathology, as described by Lindberg et al [7] The body condition score was determined by two clinicians,

as described by Henneke et al [21], and ranged from 1

to 9, where 1 was extremely emaciated and 9 extremely overweight

In addition to having fulfilled the criteria for initial screening to be included in the final study, horses had

to fulfil at least one of the following criteria: hypopro-teinaemia (defined as a serum total protein concentration

of less than 54 g/L), hypoalbuminaemia (defined as a serum albumin concentration of less than 28 g/L), a peak plasma xylose concentration of less than 1.33 mmol/L [1], increased intestinal wall thickness (>4 mm) according to ultrasonographic assessment [22] or changes in the rectal mucosal biopsy suggestive of IBD Horses were excluded from the final study if another, non-IBD cause of the pre-senting clinical signs was identified This included horses with significant intestinal sand accumulation [23], severe gastric ulceration (grades 3–4/4), evidence of infectious disease as indicated by changes in haematology and/or fibrinogen, and serum biochemical changes consistent with renal or hepatic failure

Therapeutic protocols

All horses included in the study were initially treated

with the same protocol Anthelmintics were started with

five consecutive days of fenbendazole (Axilur, MSD Animal

Health) 10 mg/kgper os (PO) once daily, followed by a

single dose of ivermectin at 0.2 mg/kg and praziquantel

at 1 mg/kg (Equimax, Virbac de Portugal) PO on day 6

Prednisolone (Prednisolon 40 mg, Leiras) at 1 mg/kg PO

once daily was started on day 1 and continued until the first

follow-up examination was performed, after approximately

three weeks of treatment

On follow-up, the horses were clinically evaluated, body

weight was determined by scales, and the tests previously

identified as abnormal were repeated Further medication

was decided at the treating clinician’s discretion according

to the findings from the follow-up examination and based

on the following guidelines: if the original complaint(s)

(weight loss and/or recurrent colic) had clinically improved

and the results from any/all previously abnormal tests

(D-xylose absorption, histopathology of rectal mucosal

biopsy, intestinal wall thickness as determined by

ultrason-ography, hypoalbuminaemia and/or hypoglobulinaemia)

had improved or normalised, corticosteroid therapy was

gradually tapered and then discontinued Horses that

had shown minimal or no improvement were changed

to dexamethasone (Dexametason 1.5 mg, Orion Pharma)

at 0.1 mg/kg PO once daily with subsequent treatment at

the treating clinician’s discretion Horse owners were

interviewed by telephone about their horse’s condition

and the possible reoccurrence of any symptoms

approxi-mately 3 and 6 months following the discontinuation of

treatment The national horse register database was used

to trace horses for long-term survival at three years after

the discontinuation of treatment

Statistical analysis

The Shapiro-Wilk test was used to evaluate whether the

data were normally distributed Pearson correlations were

calculated between the normally distributed parameters,

and the two-tailed Student’s t-test was used for

compari-sons between horses that were or were not alive three

years after treatment Spearman's correlation and the

Mann–Whitney U-test were used for nonparametric

data A two-tailed Fischer’s exact test was used to

com-pare the response to initial treatment between survivors

and non-survivors Significance was set at P < 0.05

Post-hoc power calculations were performed using online data

management software [24]

Results

Horses

Thirty-six client-owned horses met the criteria for initial

screening, with 20 horses subsequently included in the

final study Five of the 20 horses included in the final

study had a primary complaint of recurrent colic, nine horses were included due to weight loss and six presented with a history of both recurrent colic and weight loss

Diagnostic evaluation

Histopathology of the rectal mucosal biopsy was con-sidered abnormal in 5/13 and 3/7 of survivors and non-survivors, respectively Intestinal thickening (>4 mm),

as determined by ultrasound, was present in 6/13 and 4/7 of survivors and non-survivors, respectively These proportions did not significantly differ between survivors and non-survivors The proportion of horses with a peak D-xylose concentration below the normal threshold of 1.33 mmol/L did not differ between survivors (8/13) and non-survivors (6/7) However, the mean peak D-xylose concentration was significantly higher in survivors (1.36 ± 0.44) than non-survivors (0.94 ± 0.36) (P = 0.048) Faecal flotation was negative in all horses The presumptive diagnosis of the IBD subtype was based on the history, clinical presentation and the results of the diagnostic work-up, with particular emphasis placed on histo-pathological changes in the rectal mucosal biopsy

Treatment and follow up

Treatment was attempted in all horses and all returned for re-evaluation at approximately three weeks Five horses failed to demonstrate satisfactory improvement in their clinical or clinicopathological parameters in the first weeks and were changed to dexamethasone therapy as outlined above The remaining 15 horses were considered to have improved and corticosteroid therapy was tapered and discontinued

Seven of the 20 horses died during the three-year

follow-up period, with death related to the original problem of weight loss or recurrent colic in all but one horse (Table 1)

Of these seven horses, three had initially responded well

to treatment, while four had responded poorly The overall 3-year survival rate in horses that responded to initial treatment (12/15: 80%) was significantly higher (P = 0.031) than in horses that did not respond to initial treatment and were subsequently changed to dexamethasone (1/5: 20%) Five of the non-surviving horses underwent post-mortem examination, and in four of these horses this examination confirmed the presumptive diagnosis

of inflammatory bowel disease Table 2 presents the age, body composition score, serum protein, albumin and globulin concentration, and peak D-xylose concentra-tions at enrolment, as well as the length of treatment for survivors and non-survivors The peak D-xylose concentration correlated significantly with serum total protein (r = 0.45,P < 0.001) and globulin concentrations (r = 0.61,P = 0.005), but not with serum albumin concen-tration (r =−0.19, P = 0.41) The power of the study to

detect a difference between survivors and non-survivors

was 49.1%, 12.1% and 62.6% for serum total protein, serum

albumin and serum globulin concentrations, respectively

Discussion

In the present study, the response to anthelmintic and

corticosteroid therapy over a three-week period was

demonstrated to be a useful predictor of the outcome in

horses with a presumptive diagnosis of IBD The long-term

prognosis for horses in the present study was fair to

moderate, with 65% of the horses surviving at least

three years This is in contrast to the current literature,

in which the response of IBD to corticosteroid treatment

is generally considered to be poor [4,8,16,17] Possible

reasons for this discrepancy, including case selection,

case definition and the role of anthelmintic therapy in

the outcome, warrant discussion

Anthelmintic therapy was performed regardless of the

negative results of faecal analysis, as the faecal flotation

test underestimates the parasite burden when there are

more larval stages than adults, and is unable to detect

encysted cyathostomes [25] Furthermore, it has been

postulated that endoparasites may have a role in triggering the disease process of inflammatory bowel disease [26-28]

As such, the treatment of endoparasitism in suspected IBD cases is logical Fenbendazole was chosen as the therapeutic agent, as it is efficacious against encysted cya-thostomes when used as described above [29], and there was no known resistance towards fenbendazole in the geographical area in which the study was performed Although both hospitals involved in the study were referral centres, the case load at both facilities is a broad representation of the clinical spectrum, with a large proportion of the case load effectively comprising first opinion cases The inclusion of first opinion cases may

at least partly explain the better outcome observed in the study than previously reported Similarly, most of the cases in the present study that were presumptively diagnosed with IBD were less severely affected than the confirmed cases described in the literature [8,30,31] This may have biased the population studied towards animals that were more likely to respond to treatment than those previously reported from true referral popu-lations [4,8,16,17] Alternatively, it is possible that the

Table 1 Presumptive IBD subtype (based on the clinical picture and findings from the diagnostic work-up) and

post-mortem diagnoses (when available) of non-survivors (n = 7), and length of survival after the discontinuation

of treatment

Lymphocytic-plasmacytic enteritis During the treatment (day 26) Progressive weight loss,

animal welfare

Lymphocytic-plasmacytic enteritis Eosinophilic enterocolitis 2 days after discontinuing the treatment Colic Idiopathic small intestinal

muscular hypertrophy Eosinophilic enterocolitis 22 days after discontinuing the treatment Death due to acute cardiac failure Eosinophilic enterocolitis

Acute cardiac failure Eosinophilic enterocolitis 30 days after discontinuing the treatment Colic Not performed

Lymphocytic-plasmacytic enteritis 120 days after discontinuing the treatment Progressive weight loss Lymphocytic-plasmacytic enteritis Eosinophilic enterocolitis 7 months 13 days after discontinuing

the treatment

Eosinophilic enterocolitis 1 year 8 months after discontinuing

the treatment

Recurrent colic Eosinophilic enterocolitis

Table 2 Means ± SD (min–max) of the age, body composition score, serum protein, albumin and globulin concentrations, and peak xylose concentration, the numbers of horses with each abnormal finding and the length of treatment in

long-term (3 years) survivors and non-surviving horses

1

Data missing from two surviving horses.

2

response to treatment seen in some cases was due to

the larvicidal anthelmintic treatment that was included

in the protocol rather than the corticosteroids All

horses in the present study had a history of adequate

anthelmintic treatment, and no significant parasite burdens

were detected on faecal analysis, reducing the likelihood

that endoparasites were a major factor However, neither

factor excludes parasitism as a potential diagnosis,

espe-cially cyathostomiasis, as discussed above

The authors recognise that the definition of IBD used

in this study is broad and may inadvertently encompass

other disease conditions such as low-grade cyathostomiasis

However, despite the limitations in ruling out parasitism

and achieving a definitive diagnosis, we believe that present

study accurately reflects the clinical presentation of weight

loss and recurrent colic seen in practice As such, we argue

that the results of the study are applicable to the clinical

setting The finding that the response to initial treatment is

predictive of long-term survival is of particular importance

and direct clinical relevance The development of clearer

guidelines for the diagnosis of IBD would be beneficial in

defining inclusion criteria for future prospective studies

The results of this study support the use of the D-xylose

test in the diagnostic evaluation of recurrent colic and

weight loss, with inadequate D-xylose absorption the only

significant clinicopathological prognosticator of survival

identified Importantly, the horse’s diet can influence

the D-xylose curve, with horses fed a high-energy diet

reported to have lower peak plasma concentrations

[32] Additionally, prolonged fasting (72–96 h) can lower

the peak concentration of D-xylose [33] and warrants

consideration in the interpretation of the test results

In the present study, all the horses were fed in a similar

manner, with none receiving a high-energy diet, and no

horses were fasted for a prolonged period before testing

As such, these factors are unlikely to have influenced the

accuracy of the test

In the present study, peak D-xylose concentrations

were not associated with the serum albumin concentration,

but were associated with the serum globulin concentration

This contradicts the existing literature, wherein it is

com-monly assumed that horses with malabsorption will also

have a low serum albumin concentration, since the rate

of albumin production is slower compared to globulin

production [34] This assumption is supported by a recent

study in which both hypoproteinaemia and

hypoalbumi-naemia, but not hypogammaglobulihypoalbumi-naemia, were

associ-ated with non-survival in horses with unexplained weight

loss [14] The small number of horses in the present study

is a significant limitation, and the power of the study to

detect a difference between survivors was only 49.1%,

12.1% and 62.6% for serum total protein, serum albumin

and serum globulin concentrations, respectively As such,

the risk of a type II error was relatively high in the present

study The trend towards a difference between survivors and non-survivors in serum total protein, which is consis-tent with a recent report [14], and in serum globulins, which has not previously been reported, warrants consi-deration in the interpretation of results, although care should be taken in drawing firm conclusions

Interestingly, despite hypoalbuminaemia previously be-ing identified as a significant risk factor for non-survival

in a previous study [14], the data from the present study

do not support a similar conclusion The reasons for this discrepancy are not immediately apparent Both the present study and the previous study by Metcalfe et al [14] reporting the outcome of chronic gastrointestinal disease were limited by small numbers The risk of both type I and type II statistical errors increases as a function

of decreasing sample size, and consequentially power [35] As such, the inability to find an association between serum albumin and the outcome in the present study, or the association previously reported by Metcalfeet al [14], could be erroneous due to a type II or type I statistical error, respectively Considering this, a larger prospective clinical study is warranted to further investigate the rela-tionship between clinicopathological parameters and the outcome before any firm conclusions can be drawn How-ever, combining the results of the present study with the previous observations of Metcalfe et al [14], serum total protein appears to be the most consistent clinicopatholo-gical predictor of the outcome

Histopathological changes in the rectal biopsy were detected in less than half of the cases studied, but the findings of the present study suggest that when present, changes in rectal mucosal histopathology were in line with subsequent post-mortem findings This supports their use in the diagnostic evaluation of weight loss and/

or recurrent colic cases

Conclusions

The overall prognosis for long-term survival in horses with a presumptive diagnosis of IBD appears to be fair

to moderate The initial response to anthelmintic and corticosteroid therapy could be a useful prognostic indi-cator, and the findings of the present study suggest that

a low peak xylose concentration in absorption testing is associated with a less favourable prognosis, supporting the use of this test

Competing interests The authors declare that they have no competing interests.

Authors ’ contributions

RK participated in study design, data collection and manuscript preparation.

KN collected the data and revised the manuscript BS participated in study design, data collection and manuscript revision MA performed the histopathology and participated in manuscript revision SS participated in study design, laboratory analysis and manuscript revision MR participated in study design, laboratory analysis and manuscript revision All authors read and approved the final version of the manuscript.

This study was partly supported by a grant from the Orion-Farmos Research

Foundation We would also like to acknowledge Orion Pharma for providing

the ivermectin/praziquantel preparation and Intervet (currently MSD Animal

Health) for providing the fenbendazole preparation.

Author details

1

Department of Equine and Small Animal Medicine, Faculty of Veterinary

Medicine, University of Helsinki, P.O Box 57, FI-00014 Helsinki, Finland.

2

Faculty of Veterinary Medicine, Estonian University of Life Sciences, Tartu,

Estonia 3 Pathology Unit, EVIRA, Mustialankatu 3, 00790 Helsinki, Finland.

4

Current work address: Animagi Equine Clinic Oulu, Äimärautiontie 5, 90400

Oulu, Finland.

Received: 13 November 2013 Accepted: 26 May 2014

Published: 3 June 2014

References

1 Tamzali Y: Chronic weight loss syndrome in the horse: a 60 case

retrospective study Equine Vet Educ 2006, 18:372 –380.

2 Taylor SD, Pusterla N, Vaughan B, Whitcomb MB, Wilson WD:

Intestinal neoplasia in horses J Vet Intern Med 2006, 20:1429 –1436.

3 Edwards GB, Kelly DF, Proudman CJ: Segmental eosinophilic colitis:

a review of 22 cases Equine Vet J Suppl 2000, 32:86 –93.

4 Schumacher J, Edwards JF, Cohen N: Chronic idiopathic inflammatory

bowel diseases of the horse J Vet Intern Med 2000, 14:258 –265.

5 Archer DC, Edwards GB, Kelly DF, French NP, Proudman CJ: Obstruction

of equine small intestine associated with focal idiopathic eosinophilic

enteritis: An emerging disease? Vet J 2006, 171:504 –512.

6 Perez Olmos JF, Schofield WL, Dillon H, Sadlier M, Fogarty U:

Circumferential mural bands in the small intestine causing simple

obstructive colic: a case series Equine Vet J 2006, 38:354 –359.

7 Lindberg R, Nygren A, Persson SGB: Rectal biopsy diagnosis in horses with

clinical signs of intestinal disorders; a retrospective study of 116 cases.

Equine Vet J 1996, 28:275 –284.

8 Kemper DL, Perkins GA, Schumacher J, Edwards JF, Valentine BA, Divers TJ,

Cohen ND: Equine lymphocytic-plasmacytic enterocolitis: a retrospective

study of 14 cases Equine Vet J Suppl 2000, 32:108 –112.

9 Roberts MC: The D(+) Xylose absorption test in the horse Equine Vet J

1974, 6:28 –30.

10 Bolton JR, Merritt AM, Cimprich RE, Ramberg CF, Streett W: Normal and

abnormal xylose absorption in the horse Cornell Vet 1976, 66:183 –197.

11 Mair TS, Hillyer MH, Taylor FGR, Pearson GR: Small intestinal malabsorption

in the horse: an assessment of the specificity of the oral glucose

tolerance test Equine Vet J 1991, 23:344 –346.

12 Brown CM: The diagnostic value of the D-xylose absorption test in horses

with unexplained chronic weight loss Br Vet J 1992, 148:41 –44.

13 Mayes PA, Bender DA: Gluconeogenesis and control of blood glucose.

In Harpers Illustrated Biochemistry 26th edition Edited by Murray RK,

Granner DK, Mayes PA, Rodwell VW New York: Lange Medical Books/

McGraw-Hill; 2003:154 –162.

14 Metcalfe LVA, More SJ, Duggan V, Katz LM: A retrospective study of horses

investigated for weight loss despite a good appetite (2002 –2011).

Equine Vet J 2013, 45:340 –345.

15 Johnson PJ, Goetz TE: Granulomatous enteritis and Campylobacter

bacteremia in a horse J Am Vet Med Assoc 1993, 203:1039 –1042.

16 McCue M, Davis EG, Rush BR, Cox JH, Wilkerson MJ: Dexamethasone for

treatment of multisystemic eosinophilic epitheliotropic disease in a

horse J Am Vet Med Assoc 2003, 223:1320 –1323.

17 Stämpfli H, Oliver OE: Chronic diarrhea and weight loss in three horses.

Vet Clin North Am Equine Pract 2006, 22:27 –35.

18 Cohen ND, Peloso JG: Risk factors for history of previous colic and for

chronic, intermittent colic in a population of horses J Am Vet Med Assoc

1996, 208:697 –703.

19 Tinder O: Micro-determination of xylose in plasma Analyst 1975, 100:12 –15.

20 Andrews F, Bernard W, Byars D, Cohen N, Divers T, MacAllister C,

McGladdery A, Merrit AM, Murray MJ, Orsini J, Snyder J, Vatistas N:

Recommendations for the diagnosis and treatment of equine gastric

ulcer syndrome (EGUS) Equine Gastric Ulcer Council Equine Vet J 1999,

11:262 –272.

21 Henneke DR, Potter GD, Kreider JL, Yeates BF: Relationship between condition score, physical measurements and body fat percentage in mares Equine Vet J 1983, 15:371 –372.

22 Reef VB: Adult abdominal ultrasonography In Equine Diagnostic Ultrasound Edited by Reef VB Philadelphia: WB Saunders; 1998:273 –364.

23 Kendall A, Ley C, Egenvall A, Bröjer J: Radiographic parameters for diagnosing sand colic in horses Acta Vet Scand 2008, 50:17.

24 Knowledge Center/Calculators: Arlington, VA 22201, US: DSS Research; http://www.dssresearch.com/KnowledgeCenter/toolkitcalculators/ statisticalpowercalculators.aspx.

25 Stradford CH, McGorum BC, Pickles KJ, Matthews JB: An update on cyathostomins: Anthelmintic resistance and diagnostic tools Equine Vet J

2011, 43:133 –139.

26 Roberts MC: Malabsorption syndromes in the horse Comp Cont Educ Pract Vet 1985, 7:637 –646.

27 Cohen ND, Loy JK, Craig TM, McMullan WC: Eosinophilic gastroenteritis with encapsulated nematodes in a horse J Am Vet Med Assoc 1992, 200:1518 –1520.

28 Kalck KA: Inflammatory bowel disease in horses Vet Clin North Am Equine Pract 2009, 25:303 –315.

29 Lyons ET, Drudge JH, Tolliver SC: Larval cyathostomiasis Vet Clin North Am Equine Pract 2000, 16:501 –513.

30 Bassage LH, Johnston JK, Krotec KL: Eosinophilic enterocolitis associated with recurrent colonic impactions in a mare Equine Vet J 1997, 29:322 –325.

31 Barr BS: Infiltrative intestinal disease Vet Clin North Am Equine Pract 2006, 22:1 –7.

32 Jacobs KA, Norman P, Hodgson DRG, Cymbaluk N: Effect of diet on the oral D-xylose absorption test in the horse Am J Vet Res 1982, 43:1856 –1858.

33 Freeman DE, Ferrante PL, Kronfeld DS, Chalupa W: Effect of food deprivation

on D-xylose test results in mares Am J Vet Res 1989, 50:1609 –1612.

34 Mair TS, Pearson GR, Divers TJ: Malabsorption syndromes in the horse Equine Vet Educ 2006, 18:299 –308.

35 Christley RM: Power and error: Increased risk of false positive results in underpowered studies Open Epidemiol J 2010, 3:16 –19.

doi:10.1186/1751-0147-56-35 Cite this article as: Kaikkonen et al.: Diagnostic evaluation and short-term outcome as indicators of long-term prognosis in horses with findings suggestive of inflammatory bowel disease treated with corticosteroids and anthelmintics Acta Veterinaria Scandinavica 2014 56:35.

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